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ARTICLE
Scutation asymmetries in red-footed tortoise
Chelonoidis carbonaria Spix, 1824
(Testudines: Testudinidae)
Pere M. Parés-Casanova¹; Pinzón Brando²³; Daniel Caviedes²⁴ & Arcesio Salamanca-Carreño²⁵
¹ University of Lleida, School of Agrifood and Forestry Science and Engineering, Department of Animal Science. Lleida, España.
ORCID: http://orcid.org/0000-0003-1440-6418. E‑mail: peremiquelp@ca.udl.cat
² Universidad Cooperativa de Colombia (UCC), Facultad de Medicina Veterinaria y Zootecnia. Arauca, Colômbia.
³ E‑mail: donbranpinzon@gmail.com
⁴ ORCID: http://orcid.org/0000-0001-7871-7544. E‑mail: daniel_3120@hotmail.es
⁵ ORCID: http://orcid.org/0000-0002-5416-5906. E‑mail: asaca_65@yahoo.es
Abstract. The ability of an individual to withstand random perturbations during its development is considered a good indicator
of environmental and genetic stress. A common means of assessing developmental stability is through analysis of fluctuating
asymmetry (FA) in bilateral traits. Tortoises, with their large, solid plastron, allow for measurement of body geometry. Their
bilateral shell scutes are ideal candidates for asymmetries researches. With this issue in mind we assessed, as a preliminary
study, levels of plastron scute asymmetry in a sample of 46 red-footed tortoise Chelonoidis carbonaria from Arauca, N Colombia.
We found significative fluctuating asymmetry (FA) but no directional asymmetry, the former not increasing with carapace size
and thus indicating that tortoise shells do not become increasingly asymmetrical with age, or in other words, signaling that FA
is not being influenced by pholidosis (variability of scale cover mosaic according to the development of the scutes). Asymmetry
in plastron shape, although not necessarily apparent at first glance, varied, with gender with males exhibiting higher levels
of FA than females. Although we can not identify the potential sources of variation responsible for the observed patterns of
developmental instability, we consider this detected form of asymmetry due to unfavorable environmental conditions.
Key-Words. Directional asymmetry; Fluctuating asymmetry; Pholidosis; Tortoise shell.
INTRODUCTION scale cover mosaic of turtles (pholidosis) is ar-
ranged in longitudinal rows with strict bilateral
Bilaterally asymmetrical organisms can devel- symmetry (Cherepanov, 2014). But while the shell
op different kind of asymmetries, among which as an overall structure is under selection, specif-
are fluctuating asymmetry (FA) and directional ic landmarks on the shell (such as the location of
asymmetry (DA) (Graham et al., 1993). FA is de- scute sutures), may be under less direct selection
fined as the deviation of the symmetry of an in- (Băncilă et al., 2012; Buică & Cogălniceanu, 2013;
dividual from perfect bilateral symmetry and is Cherepanov, 2014). To date, available studies of
considered a negative indicator of the individual scale asymmetries are scarce and sometimes with
ability to resist random and small developmental contradictory conclusions. For instance, Dillard
accidents (Graham et al., 1993). These develop- (Dillard, 2017) found no shell symmetric differenc-
mental accidents are generally the result of ge- es among two populations of Pseudemys species
netic or environmental stress (Auffray et al., 1999; in east central Virginia, while Claude et al. con-
Carter et al., 2009). On the other side, DA occurs sidered them negligible, too (Claude et al., 2003).
whenever there is a greater development of a But Davis & Grosse found FA in Trachemys scripta
character on one side of the plane of symmetry (Davis & Grosse, 2008), as did Băncilă et al. (2012)
than the other (Kharlamova et al., 2010; Lotto & in Testudo graeca ibera. Cherepanov (Cherepanov,
Béguelin, 2014). An important proportion of DA 2014) describes a 81% of asymmetrical horny
can have a genetic basis. pattern in his studied collection, which includ-
Tortoise shell represents the genotype by en- ed Mauremys caspica, Emys orbicularis, Testudo
vironment interaction of an individual through- graeca and Agrionemys horsfieldi, while Buică &
out its life, being this genotype susceptible to Cogălniceanu (2013) detected low levels of FA in
environmental perturbations. In a typical case, Testudo graeca. Moreover these latter authors ob-
Pap. Avulsos Zool., 2020; v.60: e20206039 ISSN On-Line: 1807-0205
http://doi.org/10.11606/1807-0205/2020.60.39 ISSN Printed: 0031-1049
http://www.revistas.usp.br/paz ISNI: 0000-0004-0384-1825
http://www.scielo.br/paz
Edited by: Marcelo Duarte
Received: 25/06/2018
Accepted: 16/07/2020
Published: 28/08/2020
Pap. Avulsos Zool., 2020; v.60: e20206039 Parés-Casanova, P.M. et al.: Scutation asymmetries in red-footed tortoise
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served no correlation of asymmetry with body size and
suggested that FA would be an individual trait, with no
predictive value at the population level. Finally, Rivera &
Claude (2008) suggested that turtle shell morphology
may be less functionally constrained in terrestrial envi-
ronments than in aquatic ones.
For the quantification of these asymmetries, both
aspects of form (i.e., size and shape) should be assessed
(Sforza et al., 1998). Size and shape mutually interact, but
the variations in the former are often larger and easier to
read than are the variations in the latter, which is more
difficult to identify and quantify (Sforza et al., 1998). The
two effects should, therefore, be separately quantified.
Several approaches have been used for this purpose. In
the present study we analyze them with geometric mor-
phometric techniques, and in the plastron of red-footed
tortoise (Chelonoidis carbonaria).
Chelonoidis carbonaria is a species from South
America, distributed from northern Paraguay and
Argentina through cis-Andean South America to Panama
(Gallego-García et al., 2015; Cacciali et al., 2016; Turtle
Taxonomy Working Group, 2017). These medium-sized
tortoises generally average 30 cm as adults, but can reach Figure 1. “Llanos Orientales”, located between the rivers Arauca, Guaviare,
over 40 cm (Barros et al., 2012). They have dark-colored, Orinoco and Piedemonte Llanero, in Colombia.
loaf-shaped carapaces (back shell) with a lighter patch in
the middle of each scute, and dark limbs with brightly is characterized by a plateau (Fig. 1). The region is locat-
colored scales that range from pale yellow to dark red, ed between the rivers Arauca, Guaviare, Orinoco and
although with a great variation in this morphological Piedemonte Llanero. Seventy-five per cent of the land is
characteristic (Barros et al., 2012) (Gallego-García et al., flat, but the eastern cordillera (mountain range) borders
2015). No sex dimorphism is observed concerning size the western side of the territory where the Sierra Nevada
(Barros et al., 2012), but population differences are recog- of the Cocuy stands. At the foot of the cordillera, the soil
nized between different regions (Barros et al., 2012). They is fertile and ideal for breeding livestock. The wet season
are frequently kept as pets, and over-collection as well as is overcast, the dry season is muggy and mostly cloudy,
habitat destruction have caused them to be vulnerable and it is hot year round. Over the course of the year, the
to extinction (Gallego-García et al., 2015). temperature typically varies from 72°F to 97°F and is
Genetic or environmental disturbances that organ- rarely below 69°F or above 102°F. Water is an important
isms can encounter during their embryonic develop- natural resource in Arauca, for there are many rivers such
ment can be evaluated by FA. Because of the rapid and as the Arauca, Casanare, Tame and Tocoragua, among
intense environmental change caused by anthropogenic others. This enormous area with low touristic impact, al-
activities in the Araucan “llanos” of Colombia, such as in- though waste dumped by multinational companies are
creasing conflicts of resource use and water quality de- the main threats to the region.
terioration, there is a growing local concern about the
ecological consequences of human activities on animal
populations. Given the need for this information, the Data collection
present study aims to examine fluctuating asymmetry
as indicator of fitness (Galeotti et al., 2005) based on the Data was obtained from 46 individuals of Chelonoidis
variation in plastral shape in Chelonoidis carbonaria from carbonaria, during the dry season of February-March
Arauca. We consider that plastron, due to its clear flat- 2018. All the field-collected specimens displayed phys-
ness, will present less coplanarity problems than cara- ical traits consistent with red-footed tortoise. All speci-
pace, although this fact has not been tested in this study. mens used in the study were adults without any detect-
able abnormalities (such as injuries by predators, or un-
usual additional scutes or plates). Twelve of them were
MATERIAL AND METHODS males (4.4‑14.0 kg) and 34 were females (1.3‑8.7 kg), with
no differences in equality of distributions between males
Area sampling and females (according to Kolmogorov-Smirnov test
(D = 0.392, p = 0.09). We collected digital pictures in the
Arauca is a department of Colombia located in the ex- field, holding the camera approximately 40‑50 cm above
treme north of the Orinoco Basin of Colombia (the “Llanos each tortoise, with the camera focused on the central
Orientales”), bordering Venezuela. Its territory covers an plastron aspect of the tortoise. It was obtained a single
area of 23,818 square kilometers. It is an ecosystem that digital photograph of each animal. To prevent distortion
Parés-Casanova, P.M. et al.: Scutation asymmetries in red-footed tortoise Pap. Avulsos Zool., 2020; v.60: e20206039
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and optical aberrations no zoom was used, and the tor- was eliminated by setting the centroid size, square root
toises were maintained without inclination, using props, of sum of squared distances between the centroid and
to any side to reduce parallax errors. Identification of gen- each landmark, the same in all specimens. Position was
der was based on the presence of a pronounced plastron excluded by putting the centroid of every specimen at
concavity. Body weight was also obtained. Three individ- the same point. Orientation was taken away by rotating
uals were not clearly sexed and they were excluded of the specimens so that square root of sum of squared distanc-
study. A standard was inserted on each image for image es between corresponding landmarks would be the min-
scalar measurement calibration. After their measurement imum. By eliminating this information, only the shape
and photographing, animals were then released at the was quantified for subsequent mathematical analysis.
site of capture. Second and third authors were respon- Bilateral symmetry can either be displayed in the
sible of this part. Images were posteriorly downloaded form of two separate mirrored copies (matching symme-
to a computer, and best landmarks for analyses selected. try), or a single structure can be symmetric in itself and
Shell length were 32.2 to 48.9 cm for males, 6.7 to 51.9 cm therefore possess an internal line or plane of symmetry
for females, so a wide range of age is supposed. (object symmetry). As a turtle shell has an internal plane
of symmetry, we based our analyses on object symme-
try. The set of original configurations and mirrored cop-
Geometric morphometrics ies (including the replicated measurements) were then
superimposed (scaled, translated, and rotated) follow-
As plastrons are symmetric structures with object sym- ing the Procrustes method of generalized least squares
metry, characterized by an axis of symmetry that partially superimposition. Measurement error (ME) is of critical
fit with the sagittal line, a landmark configuration with- importance when analyzing FA (Palmer, 1994). To assess
out landmarks along the axial plane was tested (Fig. 2). the significance of FA relative to ME, all individuals were
The final symmetric shape was then obtained from eight digitized twice on two different sessions.
landmarks (4 symmetric pairs) based on plastral sutures
and scutes, landmarks, occurring on both sides of the
plastron. These chosen landmarks were based on a previ- Statistical analyses
ous studies on tortoises (Dillard, 2017) and were chosen
in order to have a good representation of the overall shell To examine the amount of symmetric variation and
scutes shape and in a way that allow us to see import- asymmetry we used Procrustes ANOVA as usual in many
ant features of asymmetry. Each picture was digitized at studies on object symmetry (Klingenberg et al., 1998;
least twice, and an average of both configurations was Klingenberg & Monteiro, 2005). To avoid the assumption of
taken. The captured images were transformed to TpsUtil having an equal and independent variation at all points, it
software v. 1.40 (Rohlf, 2015a) and landmarks record- was performed a MANOVA test for symmetric component
ed using TpsDig v. 2.26 (Rohlf, 2010). We used TpsSmall and asymmetry. This test is used to compare the individu-
v. 1.33 (Rohlf, 2015b) to test whether the observed varia- al reflection interactions to measurement error, the latter
tion in shape was sufficiently small that the distribution estimated from the total variation of the entire landmark
of points in the tangent space can be used as a good configuration (Klingenberg, 2002). Then, the shape vari-
approximation of their distribution in shape space. Scale ation in the entire data set were assessed using principal
component analysis (PCA), based on the covariance matrix
of asymmetric components of shape variation. The first
one is the average of left and right sides and represents
the shape variation component, whereas the asymmetry
component represents the individual left-right differenc-
es (Klingenberg, 2002). Finally, differences between sex-
es were assessed performing a canonical variate analysis
(CVA), a multivariate statistical method used to find the
shape characters that best distinguish among sexes, for
both symmetric and asymmetric components. Analyses
were done with MorphoJ v. 1.06c (Klingenberg, 2011).
When needed, analyses were computed as permutation
test with 10.000 permutation runs. For all analyses, α = 0.05.
RESULTS
Figure 2. Landmarks situated (17) on sutures of plastral scutes (right: anal Analyses of the data set using TpsSmall indicated
region). As plastron is a symmetric structure with object symmetry, character- that an excellent correlation between the tangent and
ized by an axis of symmetry that passes through the landmark configuration, the shape space existed. The correlation (uncentered)
the symmetry axis could partially fit with the sagittal line, the final landmark between the tangent space, Y, regressed onto Procrustes
configuration excluded sagittal points, so remaining four paired landmarks. distance was 0.9995. There was little doubt on the ba-Pap. Avulsos Zool., 2020; v.60: e20206039 Parés-Casanova, P.M. et al.: Scutation asymmetries in red-footed tortoise
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Table 1. ANOVA Procrustes analysis of plastron size and shape of red-footed (p < 0.001) but DA was not detected (p = 0.674). MANOVA
tortoise Chelonoidis carbonaria with a significant interaction between the ef- test confirmed the presence of this FA being different be-
fects of individual and body side. The effect “side” can be interpreted as direc- tween specimens (Pillai’s trace = 6.58; p < 0.001). There
tional asymmetry and the interaction “individual*side” as fluctuating asym- was no change of symmetric components according
metry. SS = Sum of Squares; MS = Mean Squares; df = degrees of freedom. to size change, shape variables and centroid size being
found to be largely uncorrelated in the sample (3.49%;
Effect SS MS df F p p = 0.165). CVA revealed sexual differences for symmetri-
Individual 0.2753655 0.0007171 384 8.10 < 0.001 cal component (p < 0.0001), being levels higher in males.
Side 0.0005095 6.3698E‑05 8 0.72 0.674 PCA then was used with individually averaged values
Individual * Side 0.0339774 8.8483E‑05 384 1.43 < 0.001 to identify and describe the pattern of individual asym-
Error 1 0.0486097 6.2002E‑05 784 metries. The symmetric component of the variation (in-
terpreted as FA), the first two PCs accounted for 65.67% of
sis of this result, which supported the hypothesis that the total shape variation (PC1 + PC2 = 51.21% + 14.46%)
samples can be analyzed by geometric morphometric and the whole set of landmarks contribute quite equally
methods since it was proved the acceptability of the to the variation among individuals (Fig. 3).
data set for further statistical analysis. The estimate of
shape was accurate as the measurement error was small-
er than the true FA (MS values for individual x side for DISCUSSION
shape: 0.000088483 in comparison with the individual
value: 0.0007171) (Table 1). The repeat specimens clus- The use of geometric morphometrics plus multivariate
tered closely together on the principal axes relative to statistical techniques provides a graphic visualization of
the variation between individuals, suggesting measure- the morphological variation of the individuals. In this study
ment error was small and the dispersal is isotropic in na- we used geometric morphometric approach to investigate
ture. The significant interaction of individual*side (indi- the variation of body shape in a population of Chelonoidis
cating individual variation in size and shape), confirmed carbonaria. Fluctuating asymmetry (FA) provides a useful
the presence of significant presence of FA in the sample metric of within‐individual variance and is based on ran-
dom departures from perfect symmetry. The two sides of
a bilateral organism share the same genotype, yet each
experiences small, random perturbations during the de-
velopmental process (Van Valen, 1962; Tomkins & Kotiaho,
2001). These perturbations ultimately yield asymmetric
phenotypes and since the direction of asymmetry is ran-
dom in any given individual, it is described as fluctuating
(Palmer, 1996; Mancini et al., 2005). Unlike most ecological,
physiological or developmental responses, FA provides
an ideal state (i.e., perfect symmetry), making it a suitable
measure for evaluating environmental stress. However,
any real‐world population is expected to show some level
of variance due to developmental noise, therefore the null
hypothesis is that the shape (i.e., variance) of the right-left
sides of a trait’s distribution is equal for tortoises. But our
analyses showed significative degrees of plastron FA, with
a morphological differentiation among sexes.
Does this significant FA suggest a certain degree of
stress levels caused by unfavorable environmental factors,
which may directly influence plastron shape? The missing
correlation for body size and FA leaves the observed vari-
ations in asymmetry open to speculation. The breaking
of turtle pholidosis symmetry is connected with devia-
tions in ontogenesis, as signaled by Cherepanov (2014).
Aberrant symmetries are apparently not determined ge-
netically nor influence individual viability (Cherepanov,
2014). It is frequently suggested that morphological
variation of individuals may be strongly dependent upon
unfavorable environmental conditions, and in our sam-
ple a non-age-related action of potential stressors, which
Figure 3. Symmetric components of shape variation. The first two PCs of the could interfere with normal symmetrical shell production
symmetric component were used to describe the pattern of symmetric part of along growth (e.g., size increase) of animals is detected.
shape variation, that is, the variation in the averages of the original and re- In other words, such FA would emerge not from plastici-
flected landmark configurations constrained. The scores for PCs are arbitrary. ty or adaptation, but from the affected to developmentParés-Casanova, P.M. et al.: Scutation asymmetries in red-footed tortoise Pap. Avulsos Zool., 2020; v.60: e20206039
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